In 1944, Avedon began working as an advertising photographer for a department store, but was quickly endorsed by Alexey Brodovitch, who was art director for the fashion magazine Harper’s Bazaar. Lillian Bassman also promoted Avedon’s career at Harper’s. In 1945, his photographs began appearing in Junior Bazaar and, a year later, in Harper’s Bazaar.

In 1944, Avedon married 19-year-old bank teller Dorcas Marie Nowell, who later became the model and actress Doe Avedon; they did not have children and divorced in 1949. The couple summered at the gay village of Cherry Grove, Fire Island, and Avedon’s bisexuality has been attested to by colleagues and family. He was reportedly devastated when Nowell left him.

In 1946, Avedon had set up his own studio and began providing images for magazines including Vogue and Life. He soon became the chief photographer for Harper’s Bazaar. From 1950, he also contributed photographs to Life, Look and Graphis and in 1952 became Staff Editor and photographer for Theatre Arts Magazine. Avedon did not conform to the standard technique of taking studio fashion photographs, where models stood emotionless and seemingly indifferent to the camera. Instead, Avedon showed models full of emotion, smiling, laughing, and, many times, in action in outdoor settings, which was revolutionary at the time. However, towards the end of the 1950s, he became dissatisfied with daylight photography and open air locations and so turned to studio photography, using strobe lighting.

In 1951, he married Evelyn Franklin; she died on March 13, 2004. Their marriage produced one son, John Avedon, who has written extensively about Tibet.

Hollywood presented a fictional account of Avedon’s early career in the 1957 musical Funny Face, starring Fred Astaire as the fashion photographer “Dick Avery.” Avedon supplied some of the still photographs used in the production, including its most noted single image: an intentionally overexposed close-up of Audrey Hepburn’s face in which only her noted features – her eyes, her eyebrows, and her mouth – are visible.

When Diana Vreeland left Harper’s Bazaar for Vogue in 1962, Avedon joined her as a staff photographer. He proceeded to become the lead photographer at Vogue and photographed most of the covers from 1973 until Anna Wintour became editor in chief in late 1988. Notable among his fashion advertisement series are the recurring assignments for Gianni Versace, beginning with the spring/summer campaign 1980. He also photographed the Calvin Klein Jeans campaign featuring a fifteen-year-old Brooke Shields, as well as directing her in the accompanying television commercials. Avedon first worked with Shields in 1974 for a Colgate toothpaste ad. He shot her for Versace, 12 American Vogue covers and Revlon’s Most Unforgettable Women campaign. In the February 9, 1981, issue of Newsweek, Avedon said that “Brooke is a lightning rod. She focuses the inarticulate rage people feel about the decline in contemporary morality and destruction of innocence in the world.” On working with Avedon, Shields told Interview magazine in May 1992, “When Dick walks into the room, a lot of people are intimidated. But when he works, he’s so acutely creative, so sensitive. And he doesn’t like it if anyone else is around or speaking. There is a mutual vulnerability, and a moment of fusion when he clicks the shutter. You either get it or you don’t”.

In addition to his continuing fashion work, by the 1960s Avedon was making studio portraits of civil rights workers, politicians and cultural dissidents of various stripes in an America fissured by discord and violence. He branched out into photographing patients of mental hospitals, the Civil Rights Movement in 1963, protesters of the Vietnam War, and later the fall of the Berlin Wall.

A personal book called “Nothing Personal,” with a text by his high school classmate James Baldwin, appeared in 1964. During this period, Avedon also created two well known sets of portraits of The Beatles. The first, taken in mid to late 1967, became one of the first major rock poster series, and consisted of five psychedelic portraits of the group — four heavily solarized individual color portraits, and a black-and-white group portrait taken with a Rolleiflex camera and a normal Planar lens. The next year, he photographed the much more restrained portraits that were included with The Beatles LP in 1968. Among the many other rock bands photographed by Avedon, in 1973, he shot Electric Light Orchestra with all the members exposing their bellybuttons for recording On the Third Day.

Avedon had numerous museum exhibitions around the world. His first major retrospective was at the Minneapolis Institute of Arts in 1970. The Metropolitan Museum of Art, New York, presented two solo exhibitions during his lifetime, in 1978 and 2002. In 1980 another retrospective was organized by the University Art Museum in Berkeley. Major retrospectives were mounted at the Whitney Museum of American Art, New York (1994), and at the Louisiana Museum of Modern Art, Humlebaek, Denmark (2007; which traveled to Milan, Paris, Berlin, Amsterdam and San Francisco, through 2009). Showing Avedon’s work from his earliest, sun-splashed pictures in 1944 to portraits in 2000 that convey his fashion fatigue, the International Center of Photography in 2009 mounted the largest survey of his fashion work. Also in 2009, the Corcoran Gallery of Art showed Richard Avedon: Portraits of Power, bringing together his political portraits for the first time.

In 1970, Avedon purchased a former carriage house on the Upper East Side of Manhattan that would serve as both his studio and apartment. In the late 1970s, he purchased a four-bedroom house on a 7.5-acre (3.0 ha) estate in Montauk, New York, between the Atlantic Ocean and a nature preserve; he sold it for almost $9 million in 2000.

Serious heart inflammations hindered Avedon’s health in 1974. The troubling time inspired him to create a compelling collection from a new perspective. In 1979, he was commissioned by Mitchell A. Wilder (1913–1979), the director of the Amon Carter Museum in Fort Worth, Texas, to complete the “Western Project.” Wilder envisioned the project to portray Avedon’s take on the American West. It became a turning point in Avedon’s career when he focused on everyday working class subjects such as miners soiled in their work clothes, housewives, farmers and drifters on larger-than-life prints, instead of the more traditional options of focusing upon noted public figures or the openness and grandeur of the West. The project lasted five years concluding with an exhibition and a catalogue. It allowed Avedon and his crew to photograph 762 people and expose approximately 17,000 sheets of 8×10 Kodak Tri-X Pan film. The collection identified a story within his subjects of their innermost self, a connection Avedon admits would not have happened if his new sense of mortality through severe heart conditions and aging hadn’t occurred. Avedon visited and traveled through state fair rodeos, carnivals, coal mines, oil fields, slaughter houses and prisons to find subjects. In 1994, Avedon revisited his subjects who would later speak about In the American West aftermath and its direct effects. Billy Mudd, a trucker, went long periods of time on his own away from his family. He was a depressed, disconnected and lonely man before Avedon offered him the chance to be photographed. When he saw his portrait for the first time, Mudd saw that Avedon was able to reveal something about Mudd that allowed him to recognize the need for change in his life. The portrait transformed Mudd, and led him to quit his job and return to his family.

In 1982 Avedon produced a playfully inventive series of advertisements for fashion label Christian Dior, based on the idea of film stills. Featuring director Andre Gregory, photographer Vincent Vallarino and model/actress Kelly Le Brock, the color photographs purported to show the wild antics of a fictional “Dior family” living ménage à trois while wearing elegant fashions.

Avedon became the first staff photographer for The New Yorker in 1992, where his post-apocalyptic, wild fashion fable “In Memory of the Late Mr. and Mrs. Comfort,” featuring model Nadja Auermann and a skeleton, was published in 1995. Other pictures for the magazine, ranging from the first publication, in 1994, of previously unpublished photos of Marilyn Monroe to a resonant rendering of Christopher Reeve in his wheelchair and nude photographs of Charlize Theron in 2004, were topics of wide discussion. Some of his less controversial New Yorker portraits include those of Saul Bellow, Hillary Clinton, Toni Morrison, Derek Walcott, John Kerry, and Stephen Sondheim. In his later years, he continued to contribute to Egoïste, where his photographs appeared from 1984 through 2000. In 1999, Avedon shot the cover photos for Japanese-American singer Hikaru Utada’s Addicted to You.

Helen Whitney’s 1996 American Masters documentary episode, Avedon: Darkness and Light, depicts an aging Avedon identifying In the American West as his best body of work. The project was embedded with Avedon’s goal to discover new dimensions within himself, from a Jewish photographer from the East who celebrated the lives of noted public figures, to an aging man at one of the last chapters of his life, to discovering the inner-worlds, and untold stories of his Western rural subjects.

On October 1, 2004, Avedon died in a San Antonio, Texas hospital of complications from a cerebral hemorrhage. He was in San Antonio shooting an assignment for The New Yorker. At the time of his death, he was also working on a new project titled Democracy to focus on the run-up to the 2004 U.S. presidential election.

The Richard Avedon Foundation is a private operating foundation, structured by Avedon during his lifetime. It began its work shortly after his death in 2004. Based in New York, the foundation is the repository for Avedon’s photographs, negatives, publications, papers, and archival materials. In 2006, Avedon’s personal collection was shown at the Pace/MacGill Gallery, New York, and at the Fraenkel Gallery, San Francisco, and later sold to benefit the Avedon Foundation. The collection included photographs by Martin Munkacsi, Edward Steichen and Man Ray, among others. A slender volume, Eye of the Beholder: Photographs From the Collection of Richard Avedon (Fraenkel Gallery), assembles the majority of the collection in a boxed set of five booklets: “Diane Arbus,” “Peter Hujar”, “Irving Penn”, “The Countess de Castiglione” and “Etcetera,” which includes 19th- and 20th-century photographers.

The 2005 film Capote contains a recreation of Avedon photographing convicted murderers Perry Edward Smith and Richard Hickock in April 1960. Avedon is portrayed by the film’s cinematographer, Adam Kimmel.

In 2010, a record price of £719,000 was achieved at Christie’s for a unique seven-foot-high print of model Dovima, posing in a Christian Dior evening dress with elephants from the Cirque d’Hiver, Paris, in 1955. This particular print, the largest of this image, was made in 1978 for Avedon’s fashion retrospective at the Metropolitan Museum of Art in New York, and was bought by Maison Christian Dior.